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Microbial coculture holds immense promise for biomanufacturing. Herein, we designed a synthetic consortium of G. lucidum and L. plantarum for enhanced natural product biosynthesis. The spatio-temporal alignment of the strains revealed an implicit disposition for transient and long-term mutualistic co-existence in the shared environment. The consortium assembly and biomass growth were driven by an intuitive toggle-switching of carbon/nitrogen sources, multi-metabolite cross-feeding, and TOR signalling. Extracellular electron transfer propelled by redox shuttles facilitated the distribution of high-energy electrons and enhanced the consortium’s robustness. The ROS-scavenging activity of antioxidant enzymes maintained the cells’ viability via intracellular ROS removal. Small-signalling molecules stimulated the biosynthesis of bioactive natural products in the coculture. Over-expression of target genes further enhanced ganoderic acids and exopolysaccharides bioproduction in the coculture system. The study provides insight into the physicochemical and molecular forces that drive cooperative interaction and stimulate natural product biosynthesis in G. lucidum and L. planatarum consortium.